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THE RAFFLES BULLETIN OF ZOOLOGY 2011 THE RAFFLES BULLETIN OF ZOOLOGY 2011 59(2): 117–125 Date of Publication: 31 Aug.2011 © National University of Singapore

NEW SPECIES OF THE GENUS SINULARIA (OCTOCORALLIA: ALCYONACEA) FROM SINGAPORE, WITH NOTES ON THE OCCURRENCE OF OTHER SPECIES OF THE GENUS Y. Benayahu Department of Zoology, George S. Wise Faculty of Life Sciences, Tel Aviv University, Ramat Aviv, 69978, Israel [email protected]

L. P. van Ofwegen Netherlands Center for Biodiversity Naturalis, P.O. Box 9517, 2300 RA Leiden, The Netherlands [email protected]; [email protected]

ABSTRACT. – A new species of the genus Sinularia, S. choui, featuring leptoclados-type clubs, is described and depicted from Singapore coral reefs. S. acuta Manuputty & Ofwegen, 2007, featuring similar clubs, is discussed. Three other species of this genus with such clubs are listed: S. maxima Verseveldt, 1971; S. molesta Tixier-Durivault, 1970 and S. verseveldti Ofwegen, 1996. S. polydactyla (Ehrenberg, 1834) is also listed. All these species are new zoogeographical records for Singapore. The total Sinularia citation fauna of Singapore currently comprises of 18 species. KEY WORDS. – Octocorallia, Alcyonacea, Sinularia, new species, new records, coral reefs, Singapore.

type clubs. Thus, in this case the congruence between the classical taxonomy and molecular phylogeny further substantiates the validity of the leptoclados-clade as a major one among the genus. In anticipation of resolving species boundaries of this clade, especially among look-alikes, conclusions concerning the identification of some Sinularia colonies from Singapore were postponed (Benayahu & Chou, 2010: 6). Since then, further progress in the study of species belonging to this clade (e.g., Ofwegen, 2008; McFadden et al. 2009; Dautova et al., 2010) has facilitated identification of the respective specimens collected from the Singapore reefs as shown below.

INTRODUCTION A recent paper by Benayahu & Chou (2010) summarised the current status of knowledge of Singapore’s Octocorallia. That study examined a diverse collection from these reefs, which yielded 25 species of the families Alcyoniidae (21 species), Briareidae (1), Helioporidae (1), Paralcyoniidae (1) and Xeniidae (1), all found to be new zoogeographical records for Singapore. It also yielded a new species, Cladiella hartogi Benayahu & Chou, 2010, that was described and depicted. The genus Sinularia May, 1898 has been found to be the most specious among Singapore’s octocorals (Benayahu & Chou, 2010), similar to other Indo-Pacific regions (e.g., overview: Ofwegen, 2002; Okinawa: Benayahu, 2002; Taiwan: Benayahu et al., 2004; Moluccas, Indonesia: Manuputty & Ofwegen, 2007; Palau: Ofwegen, 2008; Vietnam: Dautova et al., 2010). Among the ~165 morphospecies of Sinularia, one of the largest groups of species features leptoclados-type clubs (Verseveldt, 1980). These sclerites received this name since they are typically found in S. leptoclados (Ehrenberg, 1834), one of the first described species of the genus and also considered to be common. Using the octocoral-specific mitochondrial msh1 gene, McFadden et al. (2009) constructed a molecular phylogeny for Sinularia, proposing five major clades and subclades, among which a relatively high number of species have been assigned to clade 5c, with leptoclados-

MATERIAL AND METHODS During Jul.1999, collections were conducted by the first author at Pulau [=Island] Hantu, Pulau Satumu and Terumbu Pempang Tengah (artificial reef site) in Singapore. For details of collection procedures and map see Benayahu & Chou (2010). Additional Sinularia colonies were obtained from the Zoological Reference Collection (ZRC) of the Raffles Museum of Biodiversity Research (RMBR), National University of Singapore, and are included in the current study. These colonies had been collected between 1993–1997 from Pulau Hantu, St. John’s Island and Pulau Semakau (see also Benayahu & Chou, 2010: Fig. 1). It should also be noted that since all material had been initially preserved in formalin it was not suitable for DNA analysis. The ZRC-RMBR

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Benayahu and Ofwegen: Octocorals of the genus Sinularia from Singapore Table 1. List of species of Octocorallia of the order Alcyonacea (Lamouroux, 1816), genus Sinularia May, 1898 from Singapore, with indication of inventory numbers of the Raffles Museum of Biodiversity Research (ZRC) and of the Zoological Museum Tel Aviv University (ZMTAU Co), collection sites and dates of collection. Previous ZRC numbers of material deposited at Tel Aviv University are given in square brackets. Classification Alcyoniidae Lamouroux, 1912 Genus Sinularia May, 1898 Sinularia acuta Manuputty & Ofwegen, 2007 1 colony (1999.1043), Pulau Semakau, coll. S.L.M. Teo & T.H. Choong, 12 Jun.1995; 1 colony (1999.1054), Pulau Hantu, southeast side of Is., reef flat, coll. S.L.M. Teo & C.S.C. Lee, 8 Mar.1993; 1 colony (ZRC 1999.1080), Pulau Hantu, southeast side of Is., coll. S.L.M. Teo, 16 Feb.1995; 1 colony (ZMTAU Co 35104) ) [ZRC 1999.2224], Pulau Hantu, 1–4 m, coll. Y. Benayahu, 15 Jul.1999; 1 colony (ZRC 1999.2229), Pulau Hantu, 1–4 m, coll. Y. Benayahu, 9 Jul.1999; 1 colony (1999.2268), Pulau Satumu (Raffles Lighthouse), 3–6 m, coll. Y. Benayau, 15 Jul.1999. Sinularia choui, new species Holotype (ZRC 1999.2249) and four microscopic slides deposited at TAU (ZMTAU Co 35103), Terumbu Penpang Tengah, 2–4 m, coll. Y. Benayahu, 14 Jul.1999. Sinularia maxima Verseveldt, 1971 1 colony (ZMTAU Co 35105), 1 colony [ZRC 1999.1066], Pulau Hantu, north side of Is., reef flat, coll. S.L.M. Teo & C.S.C. Lee, 30 May 1994; 1 colony (ZRC 1999.1070); Pulau Hantu, coll. S.L.M. Teo & C.S.C. Lee, 6 Oct.1994. Sinularia molesta Tixier-Durivault, 1970 2 colonies (ZRC 1999.1100), St. John’s Is. south-east side of Is., coll. C.S.C. Lee, 7 Oct.1994; 2 colonies (ZRC 1999.2226), Pulau Hantu, 1–4 m, coll. Y. Benayahu, 9 Jul.1999; 1 colony (ZMTAU Co 35106), 1 colony [ZRC 1999.2264], Pulau Satumu (Raffles Lighthouse), 3–6 m, coll. Y. Benayahu, 15 Jul.1999. Sinularia polydactyla (Ehrenberg, 1834) 1 colony (1999.1063), Pulau Hantu, north-west side of Is., coll. S.L.M. Teo & C.S.C. Lee, 23 Jun.1993. Sinularia verseveldti Ofwegen, 1996 1 colony (ZMTAU Co 35107), 3 colonies [ZRC 1999.2217], Terumbu Pempang Tengah (artificial reef site), 2 m, coll. Y. Benayahu, 8 Jul.1999.

samples lack data on collection depth. Duplicate material of the collection was deposited at the Zoological Museum, Tel Aviv University (ZMTAU) as indicated below, followed by the original ZRC collection numbers of these colonies given in square brackets.

Diagnosis. – The holotype is a stalked colony, with a maximum cross-section of 2 × 4 cm and 5 cm high (Fig. 1a). The polypary consists in densely placed lobes that bear lobules with a rounded tip. Some of the polyps are partially retracted and visible on the surface of the lobules.

Sclerites were obtained by dissolving the tissues in 10% sodium hypochlorite, and prepared for scanning electron microscopy as follows: the sclerites were carefully rinsed with double-distilled water, dried at room temperature, coated with gold, and then examined with a Jeol 6480LV electron microscope operated at 10 kV. Identification of species was in part facilitated by comparisons with permanent sclerite preparations of type material kept at the Netherlands Center for Biodiversity Naturalis, Leiden (RMNH). The specimens were deposited in ZRC-RMBR and duplicate material in ZMTAU.

The polyps have a collaret and eight points. The point sclerites have poorly developed heads, up to 0.19 mm long (Fig. 2a). The collaret spindles are slightly bent, 0.13–0.24 mm long, featuring sparse tubercles on their surface (Fig. 2b). The surface layer of the lobules has leptoclados-type clubs, 0.10–0.26 mm long, whose heads mostly feature pointed leaf-like processes (Fig. 2c). In addition, there are clubs, up to 0.24 mm long, with heads featuring a prominent warty ornamentation (Fig. 3a), and others that are even longer,

TAXONOMY The examined material yielded six Sinularia species (Table 1), including Sinularia choui, new species.

Sinularia choui, new species (Figs. 1a–4) Material examined. – Holotype (ZRC 1999.2249) and four microscope slides deposited at TAU (ZMTAU Co 35103), Terumbu Penpang Tengah, 2–4 m, coll. Y. Benayahu, 14 Jul. 1999.

Fig. 1. Sinularia from Singapore; a, Sinularia choui new species; holotype (ZRC 1999.2249); b, Sinularia acuta Manuputty & Ofwegen, 2007 (ZRC 1999.2268). Scale bar 10 mm.

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Fig. 2. Sinularia choui new species; holotype (ZRC 1999.2249): a–b, polyp sclerites; a, point-clubs; b, collaret spindles; c, clubs of surface layer of lobules with leaf-like processes. Scale bar 0.10 mm.

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Benayahu and Ofwegen: Octocorals of the genus Sinularia from Singapore

Fig. 3. Sinularia choui new species; holotype (ZRC 1999.2249): a–c, sclerites of surface layer of lobules; a, clubs with head featuring warty ornamentation; c, spindles; d, spindles of interior of lobules; e–f, tubercles on spindles. Scale bar at a and c 0.10 mm; that at a only applies to a, that at c applies to b–c; scale bar at d 1 mm only applies to d.

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Fig. 4. Sinularai choui new species; holotype (ZRC 1999.2249): a–e, sclerites of surface layer of colony base, a–e; a, clubs with leaflike processes; b–c, clubs with head featuring warty ornamentation; d, capstans; e, spindles; f, spindles of interior of base; g, tubercles on spindle. Scale bar at a and e 0.10 mm; that at a applies to a–d; that of e only applies to e; scale bar at f 1 mm.

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Benayahu and Ofwegen: Octocorals of the genus Sinularia from Singapore up to 0.38 mm (Fig. 3b). The surface of the lobes has spindles, up to 0.51 mm long, with warty tubercles that are occasionally more common at one end of the spindle than the other (Fig. 3c).

Remarks. – The discussed colonies from Singapore resemble the holotype of S. acuta, except for ZRC 1999.2268, which shows certain differences. For comparison, both the colony and sclerites of ZRC 1999.2268 are presented here (Figs. 1b, 5–7). The colony shape (Fig. 1b) corresponds to the description of the holotype (Manuputty & Ofwegen, 2007: Fig. 2a). The sclerites of the polypary fit those of the holotype, including the polyp point (Fig. 5a) and crown (Fig. 5b), the clubs of the surface layer of the lobes (Fig. 5c, d) and its spindles (Fig. 5e) (see Manuputty & Ofwegen, 2007: Fig. 3). Similarly, the sclerites of the surface layer of the base, including the clubs (Fig. 6a, b) and spindles (Fig. 6c), correspond to the holotype (Manuputty & Ofwegen, 2007: Fig. 4). However, the spindles of the interior of the lobules of ZRC 1999.2268 are mostly branched (Fig. 7a), as opposed to those of the other examined colonies (see above) and the holotype (Manuputty & Ofwegen, 2007: Fig. 4c). The tubercular ornamentation of the spindles of all the colonies corresponds to the holotype (Fig. 7b, c, e, f). Notably, even the spindles in the interior of the base of ZRC 1999.2268 occasionally feature a side branch (Fig. 7d). We consider the slender spindles of the holotype of S. acuta, which are up to 3.6 mm long, a diagnostic of the species. The spindles depicted in Fig. 7a, are indeed of this type, up to 4 mm long, yet branched. Such differences between the holotype of S. acuta and the discussed colony are considered to reflect intra-specific variation, as commonly found in other Sinularia species (e.g., Dautova et al., 2010).

The clubs with leaf-like processes on the surface layer of the colony base are 0.10–0.17 mm long (Fig. 4a). They have wider handles and are shorter compared to those of the lobules’ surface. Some of these clubs, up to 0.30 mm long, feature heads with a warty ornamentation (Fig.4b, c). In addition, there are capstan-like sclerites, 0.10–0.16 mm long (Fig. 4d). The spindles of the surface of the base are shorter than those of the surface of the lobes, up to 0.37 mm long (Fig. 4e). The interior of the lobules has spindles, up to 1.95 mm long, some bent and with a side branch (Fig. 3d). Most of the spindles have sparsely dispersed small tubercles (Fig. 3e), but a few have more densely located and larger ones (Fig. 3f). The spindles in the interior of the base are up 1.90 mm long (Fig. 4f) with a dense tubercular sculpture (Fig. 4g). Colour. – The preserved holotype is light cream. Etymology. – The species name honours Prof. L. M. Chou, National University of Singapore, a prominent coral reef scientist, in appreciation of his initiative to conduct a soft coral survey in Singapore and in recognition of his immense contribution to the study of the Singapore reefs.

DISCUSSION

Remarks. – Based on the presence of leptoclados-type clubs, collaret and point sclerites we assigned S. choui to clade 5C of McFadden et al. (2009). Within this clade, S. pumila Dautova et al., 2010 reveals two types of clubs in the surface layer of the lobes, with head either featuring pointed leaf-like processes or a warty ornamentation. In S. choui the clubs are larger than in S. pumila: the leafy ones reach up to 0.26 mm compared to 0.15 mm; the warty ones, 0.38 mm compared to 0.26 mm, respectively. Similarly, in S. choui most of the clubs of the surface layer of the base are longer than 0.10 mm (Fig. 4a), whereas in S. pumila they are 0.10 mm long or less (Dautova et al. 2010: Fig. 18). Hence, we conclude that S. choui has unique sclerite features, and does not resemble any congeneric species already described.

The present study has yielded a new species, S. choui, and another five new zoogeographical records of the genus Sinularia for Singapore’s reefs. Along with the 12 previously reported species of this genus there (Benayahu & Chou, 2010), these findings bring to a total of 18 the number of Sinularia species of Singapore. Moreover, the current results increase to 31 the number of octocoral species there, of the families Alcyoniidae, Briareidae, Heliporidae, Paralcyoniidae and Xeniidae, with the first one comprising 87% (27 species) of the total number. Although Sinularia species are prevalent on Singapore’s reefs, their diversity is lower, for example, compared to the reefs of the South China Sea (32) and Indonesia (28) (Ofwegen, 2002); while the octocorals of the Philippines have not been sufficiently studied (see also Dautova et al., 2010), it can be anticipated that the Sinularia diversity there is also quite high. Regrettably, there is also a scarcity of information on Sinularia diversity from other reefs in the region, such as those of Malaysia, the Gulf of Thailand, Brunei, Borneo, etc. Consequently, the level of diversity of the genus Sinularia in Singapore cannot be evaluated within the relevant regional scale. At this stage, therefore, it can be cautiously concluded that the number of Sinularia species on the Singapore reefs is rather moderate; a conclusion that can also be applied to the diversity of other genera of the family Alcyonacea there, as reflected in the findings of Benayahu & Chou (2010).

Sinularia acuta Manuputty & Ofwegen, 2007 (Figs. 1b, 5–7) Sinularia acuta Manuputty & Ofwegen, 2007: 193 (Ambon); Ofwegen, 2008: 635-636 (Palau). Material examined. – 1 colony (1999.1043), Pulau Semakau, coll. S.L.M. Teo & T.H. Choong, 12 Jun.1995; 1 colony (1999.1054), Pulau Hantu, south-east side of Is., reef flat, coll. S.L.M. Teo & C.S.C. Lee, 8 Mar.1993; 1 colony (ZRC 1999.1080), Pulau Hantu, south-east side of Is., coll. S.L.M. Teo, 16 Feb.1995; 1 colony (ZMTAU Co 35104) [ZRC 1999.2224], Pulau Hantu, 1–4 m, coll. Y. Benayahu, 15 Jul.1999; 1 colony (ZRC 1999.2229), Pulau Hantu, 1–4 m, coll. Y. Benayahu, 9 Jul.1999; 1 colony (1999.2268), Pulau Satumu (Raffles Lighthouse), 3–6 m, coll. Y. Benayau, 15 Jul.1999.

ACKNOWLEDGEMENTS We wish to thank L. M. Chou for initiating the octocoral survey in Singapore and inviting Y. Benayahu to perform

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Fig. 5. Sinularia acuta Manuputty & Ofwegen, 2007 (ZRC 1999.2268): a–b, polyp sclerites; a, point-clubs; b, collaret spindles; c–e, sclerites of surface layer of lobules; c–d, clubs; e spindles. Scale bar 0.10 mm.

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Benayahu and Ofwegen: Octocorals of the genus Sinularia from Singapore from Nha Trang Bay, South China Sea, Vietnam. Zoologische Mededelingen Leiden, 84: 47–92.

it. We are particularly grateful to the members of the Reef Ecology Study Team, Department of Biological Sciences, National University of Singapore: Lim Liang Jim, Uma Sachidhanandam, Angela Dikou, James Guest, Sukee Hajisamae, Sasi Nayar, Koh Li Ling and Adelene Tay Hwee Boon for help during the field work. We wish to thank M. Weise for technical assistance, A. Shlagman for the professional curatorial skills, V. Wexler for digital editing and N. Paz for skillful editorial assistance. The first author was supported by a “Raffles Museum Research Fellowship” from the Raffles Museum of Biodiversity Research to carry out the field surveys in Singapore. This research was in part supported by The Israel Cohen Chair in Environmental Zoology to Y.B.

Ehrenberg, G. G., 1834. Beiträge zur physiologischen Kenntniss der Corallenthiere im allgemeinen, und besonders des Rothen Meeres, nebst einem Versuche zur physiologischen Systematik derselben. Abhandl. K. Akademie der Wissenschaften, Berlin, 1832(1): 225–380. Ofwegen, L.P. van, 1996. Octocorallia from the Bismarck Sea (Part II). Zoologische Mededelingen Leiden, 70: 207–215. Ofwegen, L. P. van, 2002. Status of knowledge of the Indo-Pacific soft coral genus Sinularia May, 1988 (Anthozoa, Octocorallia). Proc. 9th Int. Coral Reef Symposium, Bali 2000, 1: 167–171. Ofwegen, L.P. van, 2008. The genus Sinularia (Octocorallia: Alcyonacea) at Palau, Micronesia. Zoologische Mededelingen Leiden, 82: 631–735. Manuputty A. E. W. & L. P. van Ofwegen, 2007. The genus Sinularia (Octocorallia: Alcyonacea) from Ambon and Seram (Moluccas, Indonesia). Zoologische Mededelingen Leiden, 81: 187–216.

LITERATURE CITED Benayahu, Y., 2002. Soft corals (Octocorallia: Alcyonacea) of the southern Ryukyu Archipelago: The families Tubiporidae, Clavulariidae, Alcyoniidae and Briareidae. Galaxea JSRS, 4: 1–21.

McFadden, C.S., L.P. van Ofwegen, E. J. B. Beckman, Y. Benayahu & P. Alderslade. 2009. Molecular systematics of the specious Indo-Pacific soft coral genus, Sinularia (Anthozoa: Coelenterata). Invertebrate Biology, 128: 303–323.

Benayahu, Y., M.-S. Jeng, S. Perkol-Finkel & C.-F. Dai, 2004. Soft corals (Octocorallia, Alcyonacea) from Southern Taiwan. II. Species diversity and distributional patterns. Zoological Studies, 43: 548–560.

Tixier-Durivault, A., 1970. Les Octocoralliaires de NouvelleCalédonie. — L’Expédition française sur les récifs coralliens de la Nouvelle-Calédonie sous l’égide de la fondation SingerPolinac 1960-1963, 4: 171–350.

Benayahu, Y. & L. M. Chou, 2010. On some octocorallia (Cnidaria: Anthozoa: Alcyonacea) from Singapore, with a description of a new Cladiella species. The Raffles Bulletin of Zoology, 58: 1–13.

Verseveldt, J., 1971. Octocorallia from North-Western Madagascar (Part II). Zoologische Verhandelingen Leiden, 117: 1–73. Verseveldt, J., 1980. A revision of the genus Sinularia May (Octocorallia, Alcyonacea). Zoologische Verhandelingen Leiden, 179: 1–128.

Dautova, T. N., L. P. van Ofwegen & O. V. Savinkin, 2010. New species of the genus Sinularia (Octocorallia: Alcyonacea)

Fig. 6. Sinularia acuta Manuputty & Ofwegen, 2007 (ZRC 1999.2268): a–c. sclerites of surface layer of base; a–b, clubs; c, spindles. Scale bar 0.10 mm.

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Fig. 7. Sinularia acuta Manuputty & Ofwegen, 2007 (ZRC 1999.2268): a, spindles of interior of lobes; b–c, tubercles on spindles of interior of lobes; d, spindles of interior of colony-base; e–f, tubercles on spindles of interior of colony-base. Scale bar 1 mm at a, also applies to d.

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